Presumed inhibitory neurons in the macaque inferior temporal cortex: visual response properties and functional interactions with adjacent neurons.

Neurons in area TE of the monkey inferior temporal cortex respond selectively to images of particular objects or their characteristic visual features. The mechanism of generation of the stimulus selectivity, however, is largely unknown. This study addresses the role of inhibitory TE neurons in this process by examining their visual response properties and interactions with adjacent target neurons. We applied cross-correlation analysis to spike trains simultaneously recorded from pairs of adjacent neurons in anesthetized macaques. Neurons whose activity preceded a decrease in activity from their partner were presumed to be inhibitory neurons. Excitatory neurons were also identified as the source neuron of excitatory linkage as evidenced by a sharp peak displaced from the 0-ms bin in cross-correlograms. Most inhibitory neurons responded to a variety of visual stimuli in our stimulus set, which consisted of several dozen geometrical figures and photographs of objects, with a clear stimulus preference. On average, 10% of the stimuli increased firing rates of the inhibitory neurons. Both excitatory and inhibitory neurons exhibited a similar degree of stimulus selectivity. Although inhibitory neurons occasionally shared the most preferred stimuli with their target neurons, overall stimulus preferences were less similar between adjacent neurons with inhibitory linkages than adjacent neurons with common inputs and/or excitatory linkages. These results suggest that inhibitory neurons in area TE are activated selectively and exert stimulus-specific inhibition on adjacent neurons, contributing to shaping of stimulus selectivity of TE neurons.

[1]  G. N. Lance,et al.  A General Theory of Classificatory Sorting Strategies: 1. Hierarchical Systems , 1967, Comput. J..

[2]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[3]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[4]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[5]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[6]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[7]  H. L. Bryant,et al.  Correlations of neuronal spike discharges produced by monosynaptic connections and by common inputs. , 1973, Journal of neurophysiology.

[8]  D. V. van Essen,et al.  Cell structure and function in the visual cortex of the cat , 1974, The Journal of physiology.

[9]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[10]  D. Simons Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[11]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[12]  K. Tanaka,et al.  Cross-Correlation Analysis of Interneuronal Connectivity in cat visual cortex. , 1981, Journal of neurophysiology.

[13]  M. E. Lewis,et al.  Opiate receptor gradients in monkey cerebral cortex: correspondence with sensory processing hierarchies. , 1981, Science.

[14]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Aertsen,et al.  Evaluation of neuronal connectivity: Sensitivity of cross-correlation , 1985, Brain Research.

[16]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[17]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  E. Fetz,et al.  Intracortical connectivity revealed by spike-triggered averaging in slice preparations of cat visual cortex , 1988, Brain Research.

[20]  H. Swadlow Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties. , 1988, Journal of neurophysiology.

[21]  H. Tamura,et al.  Inhibition contributes to orientation selectivity in visual cortex of cat , 1988, Nature.

[22]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[23]  H. Tamura,et al.  Horizontal interactions between visual cortical neurones studied by cross‐correlation analysis in the cat. , 1991, The Journal of physiology.

[24]  E. Fetz,et al.  Synaptic Interactions between Cortical Neurons , 1991 .

[25]  D. Whitteridge,et al.  An intracellular analysis of the visual responses of neurones in cat visual cortex. , 1991, The Journal of physiology.

[26]  Keiji Tanaka,et al.  Coding visual images of objects in the inferotemporal cortex of the macaque monkey. , 1991, Journal of neurophysiology.

[27]  C G Gross,et al.  Stimulus selectivity and state dependence of activity in inferior temporal cortex of infant monkeys. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[28]  R. Foehring,et al.  Correlation of physiologically and morphologically identified neuronal types in human association cortex in vitro. , 1991, Journal of neurophysiology.

[29]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[31]  S Yamane,et al.  Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  H. Tamura,et al.  Development of local horizontal interactions in cat visual cortex studied by cross-correlation analysis. , 1993, Journal of neurophysiology.

[33]  K. Rockland,et al.  Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. , 1993, Cerebral cortex.

[34]  TJ Gawne,et al.  How independent are the messages carried by adjacent inferior temporal cortical neurons? , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[36]  T. Bonhoeffer,et al.  Relationship Between Lateral Inhibitory Connections and the Topography of the Orientation Map in Cat Visual Cortex , 1994, The European journal of neuroscience.

[37]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[38]  P S Goldman-Rakic,et al.  Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  R Vogels,et al.  Responses of monkey inferior temporal neurons to luminance-, motion-, and texture-defined gratings. , 1995, Journal of neurophysiology.

[42]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[43]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[44]  E. Fetz,et al.  Synaptic Interactions between Primate Precentral Cortex Neurons Revealed by Spike-Triggered Averaging of Intracellular Membrane Potentials In Vivo , 1996, The Journal of Neuroscience.

[45]  C. Gray,et al.  Heterogeneity in local distributions of orientation-selective neurons in the cat primary visual cortex , 1996, Visual Neuroscience.

[46]  J. Deuchars,et al.  Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. , 1996, The Journal of physiology.

[47]  H. Tamura,et al.  Mechanisms underlying orientation selectivity of neurons in the primary visual cortex of the macaque. , 1996, The Journal of physiology.

[48]  C. Gray,et al.  Physiological properties of inhibitory interneurons in cat striate cortex. , 1997, Cerebral cortex.

[49]  Sulli Popilskis,et al.  Anesthesia and Analgesia in Nonhuman Primates , 1997 .

[50]  Dennis F. Kohn,et al.  Anesthesia and analgesia in laboratory animals , 2008 .

[51]  Hiroshi Tamura,et al.  A microelectrode positioning system for semiautomatically tracking neuronal spikes , 1998, Proceedings of the 20th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Vol.20 Biomedical Engineering Towards the Year 2000 and Beyond (Cat. No.98CH36286).

[52]  N. Logothetis,et al.  Functional imaging of the monkey brain , 1999, Nature Neuroscience.

[53]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[54]  J. Okada,et al.  Multineuronal spike classification based on multisite electrode recording, whole-waveform analysis, and hierarchical clustering , 1999, IEEE Transactions on Biomedical Engineering.

[55]  P. Goldman-Rakic,et al.  Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. , 1999, Journal of neurophysiology.

[56]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[57]  I. Fujita,et al.  Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex , 2000, Nature Neuroscience.

[58]  J. Hegdé,et al.  Selectivity for Complex Shapes in Primate Visual Area V2 , 2000, The Journal of Neuroscience.

[59]  I. Fujita,et al.  Disparity selectivity of neurons in monkey inferior temporal cortex. , 2000, Journal of neurophysiology.

[60]  K. Kawasaki Quantitative comparison of intrahemispheric and interhemispheric responses of neurons in macaque area TE , 2000 .

[61]  K. Miyata Interhemispheric projection between area TEs of macaque inferior temporal cortex , 2000 .

[62]  G. Orban,et al.  Three-Dimensional Shape Coding in Inferior Temporal Cortex , 2000, Neuron.

[63]  Christopher C. Pack,et al.  Dynamic properties of neurons in cortical area MT in alert and anaesthetized macaque monkeys , 2001, Nature.

[64]  P. Goldman-Rakic,et al.  Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex , 2001, The Journal of Neuroscience.

[65]  H. Tamura,et al.  Visual response properties of cells in the ventral and dorsal parts of the macaque inferotemporal cortex. , 2001, Cerebral cortex.

[66]  Y. Yamane,et al.  Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns , 2001, Nature Neuroscience.

[67]  H. Tamura,et al.  Contribution of GABAergic inhibition to receptive field structures of monkey inferior temporal neurons. , 2002, Cerebral cortex.

[68]  I. Fujita The inferior temporal cortex: Architecture, computation, and representation , 2002, Journal of neurocytology.

[69]  H. Tamura,et al.  Visual response properties of presumed inhibitory neurons in the macaque inferior temporal cortex , 2002 .

[70]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[71]  P. Goldman-Rakic,et al.  A role for inhibition in shaping the temporal flow of information in prefrontal cortex , 2002, Nature Neuroscience.

[72]  Lyle J. Graham,et al.  Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons A Diversity of Combinations Produces Spike Tuning , 2003, Neuron.

[73]  Yusuke Murayama,et al.  Coding of visual patterns and textures in monkey inferior temporal cortex , 2003, Neuroreport.

[74]  R. Shapley,et al.  Dynamics of Orientation Selectivity in the Primary Visual Cortex and the Importance of Cortical Inhibition , 2003, Neuron.

[75]  R. Freeman,et al.  Stereoscopic depth processing in the visual cortex: a coarse-to-fine mechanism , 2003, Nature Neuroscience.

[76]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[77]  U. Eysel,et al.  GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex , 2004, Experimental Brain Research.

[78]  W. J. Melssen,et al.  Detection and estimation of neural connectivity based on crosscorrelation analysis , 1987, Biological Cybernetics.

[79]  E. K. Miller,et al.  Functional interactions among neurons in inferior temporal cortex of the awake macaque , 2004, Experimental Brain Research.

[80]  D. Whitteridge,et al.  Physiological and morphological properties of identified basket cells in the cat's visual cortex , 2004, Experimental Brain Research.

[81]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.

[82]  D. A. Tigwell,et al.  On the use of isofluorane as an anaesthetic for visual neurophysiology , 2005, Experimental Brain Research.

[83]  P. Dean,et al.  Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties , 2006, Experimental Brain Research.